7
The Future of Agricultural Biotechnology

The application of biological sciences in agriculture has become increasingly prominent in the past decade. Genes were first inserted into corn using molecular techniques in 1989, and by the late 1990s farmers were growing millions of acres of transgenic corn. Clearly, the science of biotechnology for agriculture is in its infancy, yet it shows an influence beyond its years.

The previous chapters review what is known about the environmental impact of commercialized transgenic crops and approaches for monitoring that might be adapted to screen for their unanticipated effects. One key finding is that particular phenotypic characteristics of a given transgenic plant determine its likely environmental interactions; the fact that recombinant DNA methods were used in its development only indirectly affects these interactions by influencing the phenotypic characteristics of the transgenic plant. Indeed, the significance of biotechnology for environmental risk resides primarily in the fact that a much broader array of phenotypic traits can be incorporated into crop plants than was possible about a decade ago. As such, our experience with the few herbicide-tolerant and insect- and disease-resistant varieties that have been commercialized to date provides a very limited basis for predicting questions needed to be asked when future plants with very different phenotypic traits are assessed for environmental risks.

This chapter is divided into three major sections. The first includes an overview discussion of some new kinds of transgenic crops and a selective discussion of some environmental risk issues that may be associated



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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation 7 The Future of Agricultural Biotechnology The application of biological sciences in agriculture has become increasingly prominent in the past decade. Genes were first inserted into corn using molecular techniques in 1989, and by the late 1990s farmers were growing millions of acres of transgenic corn. Clearly, the science of biotechnology for agriculture is in its infancy, yet it shows an influence beyond its years. The previous chapters review what is known about the environmental impact of commercialized transgenic crops and approaches for monitoring that might be adapted to screen for their unanticipated effects. One key finding is that particular phenotypic characteristics of a given transgenic plant determine its likely environmental interactions; the fact that recombinant DNA methods were used in its development only indirectly affects these interactions by influencing the phenotypic characteristics of the transgenic plant. Indeed, the significance of biotechnology for environmental risk resides primarily in the fact that a much broader array of phenotypic traits can be incorporated into crop plants than was possible about a decade ago. As such, our experience with the few herbicide-tolerant and insect- and disease-resistant varieties that have been commercialized to date provides a very limited basis for predicting questions needed to be asked when future plants with very different phenotypic traits are assessed for environmental risks. This chapter is divided into three major sections. The first includes an overview discussion of some new kinds of transgenic crops and a selective discussion of some environmental risk issues that may be associated

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation with the next generation of transgenic crops. The second section focuses on policy, beginning with a general discussion of the context in which environmental risk from transgenic crops should be framed and then moving on to specific topics that may arise as policies for the next generation of transgenic crops evolve. The final section is a discussion of some research needs to address future issues. THE NEXT TRANSGENIC CROPS This section describes anticipated future transgenic crops, including some expected to be commercialized in the next couple of years, others that may reach commercial status on a midterm horizon sometime during the next decade, and others that are mere twinkles of ideas for transgenic crops that will require research breakthroughs before they can reach fruition. As discussed in Chapter 2, it is not possible to characterize the environmental hazards that may be associated with all such crops in advance of knowledge about their phenotypic characteristics and the agricultural ecology of the settings in which they will be grown. However, the second part of this section offers a preliminary discussion of some representative environmental risk issues that may be associated with these new transgenic crops. An Inventory of New Transgenic Crops The first commercially produced transgenic crops were based on single-gene traits. Among these was the “Flavr-Savr” tomato, which used gene silencing to inhibit the expression of an enzyme involved in fruit ripening (Kramer and Redenbaugh 1994). The Flavr-Savr tomato was not a commercial success, but the technology was effective because the fruit not only had a slow rate of ripening but also was less susceptible to pathogen infection. Other early transgenic products were based on traits influencing agronomic performance (i.e., pathogen, insect, and herbicide resistance). The rapid and broad use by the American farmer of glyphosate-resistant soybeans and Bt-expressing cotton and corn attests to the commercial success of these transgenic crops (James 1998, USDA-NASS 2001). Based on the successes of these initial transgenic crops, research laboratories throughout the world are now studying a wide variety of traits/ genes that could greatly expand the spectrum of products from such plants. As was true of the first genetically engineered crops, the rate at which new transgenic traits can be expected to appear in the future depends largely on the number of genes encoding them. So traits controlled by single genes, or traits that can be reduced or eliminated by the loss of

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation expression through gene silencing of a single gene or group of related genes, are likely to become the first available. The next logical step for expansion is the integration of single-gene traits. Crops with a set of single genes for a number of distinct traits already are in use. We can only speculate about the number of genes controlling the development and architecture of plants and the various physiological processes impacting yield. It seems safe to assume, though, that genetically complex traits will require additional years of research to understand, let alone express and regulate in a genetically engineered crop species. Nevertheless, complex traits, including those controlling adaptation to abiotic stresses, such as drought and salinity, flowering and reproduction, and hybrid vigor, are being actively investigated, and it would not be surprising if some of these could be regulated in crop plants by genetic engineering within the next 5 to 10 years. These products have the potential to not only improve agronomic performance but also increase the nutritional value of grains consumed by humans and livestock, eliminate allergens and antinutritional factors, improve the shelf life of fruits and vegetables, and increase the concentration of vitamins and micronutrients found in seeds, creating healthier foods (Abelson and Hines 1999). While there are many different kinds of transgenic crops under development, most aim to address one of four broad social needs: improved agricultural characteristics, greater adaptation to postharvest processing practices, improved food quality and other uses of value for humans, and better mitigation of environmental pollution. Indeed, so many traits currently under investigation could become incorporated into transgenic plants that space limits consideration here to only a few. Improved Agricultural Characteristics Among the transgenic traits near commercial release are new Bt genes that provide protection against additional types of insect pests. One of these is a gene that protects corn against corn rootworm damage (Kishore and Shewmaker 1999). It is estimated that damage to corn roots by this pest result in losses approaching $1 billion annually. By reducing the impact of this pest, it is expected that not only will there be better corn yields but also better drought tolerance and fertilizer utilization due to the healthier root system. Research is also being done to genetically engineer tree crops to make them resistant to insects and herbicides and to increase their rate of growth. For example, a Bt gene has been inserted into hybrid poplars to protect them against defoliation by a leaf beetle. Acreage of hybrid poplars has increased because of their good wood pulp characteristics, but they have been susceptible to insect attack, which has

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation prompted applications of insecticides. Many of these new traits for improving agricultural production on farm are ones that could have environmental impacts that are similar in kind to the present generation of transgenic crops. Their value accrues directly to the farmer and the seed company and only indirectly to other sectors of society. Their potential risks, however, are borne by a wider segment of society. Thus, risk analysis of this next generation of traits is likely to resemble present discussions and debates about biotechnology. The evaluation of these risks is likely to become more complicated and difficult as the range of transgenic crops expands from the major grain crops to the more wild and perennial plants, such as pines and poplar. Over the long term, new knowledge regarding the physiology and development of plants and their interaction with microorganisms could eventually provide the foundation to modify plant structure and reproduction. It may become possible to genetically engineer crop plants that are more tolerant to drought, salinity, and other abiotic stresses (see below); that are able to grow more efficiently in the acidic, aluminum-containing soils found in tropical areas (Herrera-Estrella 1999); that can compete more effectively with weeds; that can reproduce in a shorter time; and that can potentially fix their own nitrogen. Improved Postharvest Processing Transgenic technology is also being applied to several commercially important tree species, including poplar, eucalyptus, aspen, sweet gum, white spruce, walnut, and apple (Kais 2001). The global demand for wood and wood products is growing along with the human population. To reduce pressure on existing forests, forest plantations that grow transgenic trees are expected to play an increasingly important role in meeting the demand for tree products (Tzfira et al. 1998). As mentioned above, the first traits being genetically engineered into trees are herbicide tolerance and insect resistance, which are useful for establishing and maintaining young trees. Several traits are under development to better adapt trees to postharvest processing, and these may become commercially available in the near future. For example, there is research under way to modify the lignin content of certain tree species, in order to improve pulping, the process by which wood fibers are separated to make paper. Reduced lignin may improve the efficiency of paper production and may reduce environmental pollution from the paper production process. To restrict the transfer of transgenic traits to wild forest and orchard tree populations, it is generally considered essential to simultaneously genetically engineer reproductive sterility. Methods currently exist to do this in crop plants (Mariani et al. 1992, Williams 1995), so this technology

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation is available. Besides restricting gene flow, sterility is expected to cause the trees to grow faster and produce more wood, since energy would not be wasted producing flowers or fruit. It is likely that this issue will be investigated by a future National Research Council (NRC) committee. There is also interest in using genetic engineering technology to turn annual crop plants into factories that produce valuable chemicals (for a recent review, see Somerville and Bonetta 2001) and antibodies (Daniell et al. 2001). Plants have the capacity to synthesize a variety of complex molecules, given the simple inputs of a few minerals, carbon dioxide, water, and sunshine. It is widely thought that plants could provide a “green” renewable source of chemicals to replace those currently obtained from petroleum. This could also be a mechanism to create new markets for plant products as well as utilize excess production of agricultural commodities. The feasibility of producing a plastic precursor, polyhydroxybutyrate, in plants, was demonstrated several years ago (Poirier et al. 1992), but this was not found to be an economically viable process. Nevertheless, there is excellent potential for mass producing a variety of fatty acids in plants that serve as precursors for valuable polymers, such as nylon. The properties of plastics that incorporate starch could also be significantly improved as more knowledge is learned about the biochemistry of starch synthesis. Research is also directed toward reducing pollution in postharvest production. For example, there is ongoing research to reduce the content of phytic acid in corn. Phytic acid stores phosphorus in the developing seed (Raboy 1997). Much of this mineral complex is not digested by livestock, so it ends up in the waste stream. Ultimately, it is released into ponds and lakes, where the phosphorus can create algal blooms (Tilman 1999b). Several molecular approaches, including genetic engineering, are being applied to reduce the phytate content of corn. Some of these new plant products raise several risk issues that the first generation of products did not. If any of these applications displace crops for food and feed production, what are the marginal and aggregate effects on national and global food and feed supplies? If some applications lead to a more vertically integrated farm-to-product production system, what are the environmental impacts? These and other research questions may be important in the near future. Improved Food Quality and Novel Products for Human Use Corn and soybeans are two of the most important food and feed commodities in the United States and worldwide. Most (65 to 70%) of the 9 billion to 10 billion bushels of corn produced annually in this country are used for livestock feed; about 25% is exported, and the remaining 10%

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation is processed into food ingredients, nonfood coatings and adhesives, and ethanol (Corn Refiners Association 1999). In addition, approximately 20% of the dietary calories (of people) in the United States come from lipids obtained from plant seeds, with soybean oil accounting for about one-third of the total (www.soygrowers.wegov2.com/file_depot/0-10000000/0-10000/735/folder/4944/2000SoyStats.pdf). By altering the lipid, protein, and carbohydrate composition of these seeds, it may be possible to create more nutritious food and obtain byproducts with improved functional characteristics. Several of the transgenic products discussed below are in field trials or will soon be available for production. Corn seed has a high caloric density because of its high starch and oil content, but the protein it contains is deficient in several amino acids (lysine, methionine, tryptophan) essential for swine, poultry, and human nutrition. Transgenic corn lines that contain higher than normal levels of these amino acids and/or that produce proteins with higher contents of these acids have been created, although they are not yet in commercial production. Varieties of high-oil corn have been developed through nontransgenic technology, but transgenic technology is also being used to increase the quantity and quality of corn oil. As is also true of soybean oil (see below), the stability and nutritional value of corn oil could be improved by increasing the proportion of monounsaturated fatty acid, and there are efforts under way to do so by genetic engineering. Natural soybean oil contains a significant proportion of di- and tri-unsaturated fatty acids (linoleic and linolenic), and although these unsaturated fatty acids are generally considered healthier to eat than the saturated fatty acids found mainly in animal fat, they have a tendency to oxidize and become rancid. These unsaturated fatty acids are also liquid at room temperature, which limits their functional properties for making certain types of foods, such as margarine. The stability of soybean oil and its functional properties are improved by hydrogenating the oil. This reduces the double bonds in the unsaturated fatty acids, yielding monounsaturated trans-fatty acids. Although trans-unsaturated fatty acids have been consumed for many years, there is increasing evidence that they are unhealthy (Taubes 2001). To address this problem, soybean was genetically engineered to produce an oil that contains predominantly a cismonounsaturated fatty acid (oleic acid; Mazur et al. 1999). This was achieved through genetic engineering by silencing the genes that produce linoleic and linolenic acid from oleic acid by a desaturation reaction. The new product is soybean oil with approximately 85% monounsaturated fatty acid, which has good stability, and reduced off-flavor and is healthier to consume. The meal recovered after soybean oil has been extracted is rich in proteins that have excellent functional characteristics for creating a vari-

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation ety of foods. However, several of the most abundant soy proteins are deficient in sulfur-containing amino acids (methionine and cysteine), which are essential amino acids for humans and certain livestock. Other soy proteins are antinutritional factors, and one is a common food allergen (Ogawa et al. 1993). Thus, transgenic research has been done to remove the anti-nutritional factors and allergenic proteins from soybeans and to improve its protein quality (Mazur et al. 1999). The deficiency in the sulfur-containing essential amino acids in soy protein cannot be addressed through conventional breeding because better genes simply do not exist in the natural gene pool. However, the problem can be approached through genetic engineering by altering the activity of the enzymes that synthesize methionine and cysteine or by overproducing a protein that contains them. A complementary approach is to block expression of the major soy proteins that lack methionine and cysteine, thereby increasing the percentage of these amino acids in the remaining proteins. Both of these strategies are being explored. The feasibility of producing a methionine-rich protein in transgenic soybeans and other pulse seeds has been demonstrated (Altenbach et al. 1989, Nordlee et al. 1996), but the trait has not been commercialized. Gene silencing has been shown to be an effective way to eliminate the major soybean allergen (Jung, 2001, personal communication), and other anti-nutritional proteins have been removed by mutagenesis (Mazur et al. 1999). The promoter used to silence the fatty acid desaturase genes in the high oleic acid transgeneic soybean effectively eliminates expression of one of the major classes of soy proteins that does not contain methionine and cysteine. Consequently, the transgenic seed that was modified for high oleic acid content also has an improved protein quality. In addition to the macronutrients, starch, protein, and oil, plant foods provide many of the micronutrients essential in human diets. There are 17 minerals and 13 vitamins required at minimum levels to prevent nutritional disorders (DellaPenna 1999), and all of these have attracted biotechnology research. Clinical and epidemiological studies show an important role in health maintenance for several minerals (iron, calcium, selenium, and iodine) and vitamins (A, B6, E, and folate), but these are typically not present in sufficient quantities in many diets throughout the world. Common reliance on rice, wheat, maize, and soybean for macronutrients limits the diets of many people to the micronutrients these seeds contain. In particular, these foods are deficient in iron, zinc, selenium, copper, riboflavin, and vitamins A and C. More than two billion people face serious dietary problems due to inadequate quantities of micronutrients. For example, iron deficiency leads to anemia in 40% of all women and 50% of pregnant women and is thought to cause up to 40% of the half-million deaths at childbirth each

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation year (Welch et al. 1997). Inadequate iron in children’s diets impairs mental development. Vitamin A deficiency is considered a global epidemic (Ye et al. 2000). Annually, 250 million children suffer from vitamin A deficiency, which contributes to illness and death for some 10 million people annually. Vitamin A deficiency causes blindness in up to half a million children each year, half of whom die after losing their sight. Besides impairing vision, vitamin A deficiency can lead to protein malnutrition and poor immune system function. Folic acid deficiency increases the risk of birth defects, heart disease, and stroke. Much remains to be learned about the uptake and accumulation of minerals and the synthesis of vitamins in plants, but significant progress is being made in some areas of research, such that transgenic plants producing increased levels of several micronutrients have been created. For example, mulled rice grains contain no beta-carotene, but it has been genetically engineered by the introduction of three genes, one from daffodil and two from bacteria, to produce significant levels of beta-carotene, which is made into vitamin A (Ye et al. 2000). Additional genetic engineering may be necessary to raise the beta-carotene level in transgenic rice such that a daily serving provides the recommended daily allowance (RDA) of vitamin A. The efficacy of this approach to reducing vitamin A deficiencies remains controversial (Nestle 2001). Similar genetic approaches were used to increase the level of tocopherol, the lipid-soluble antioxidant known as vitamin E, in plant oils. The RDA for vitamin E is 10 to 13.4 international units (equal to about 7 to 9 mg of a-tocopherol), which is generally accessible through consumption of plant-derived dietary components, including soybean oil. However, an excess intake of vitamin E (100 to 1,000 IU/day) has been found to be associated with a reduced risk of cardiovascular disease and some cancers, improved immune function, and reduced progression of several human degenerative conditions (Traber and Sies 1996). Thus, there could be health benefits from increasing the level of vitamin E in commonly consumed foods, such as soybean (DellaPenna 1999). By overexpressing the gene responsible for the last step in vitamin E synthesis in the model plant Arabidopsis thaliana, the effective vitamin E level was increased nearly 10-fold (Shintani and DellaPenna 1998). A similar approach is now being used to create transgenic soybean and canola plants with enhanced levels of vitamin E. Plants contribute a number of other health-promoting chemicals to our diet (DellaPenna 1999). The glucosinolates found in broccoli and related cruciferous vegetables are thought to help detoxify cancer-inducing carcinogens (Talalay and Zhang 1996). The isoflavones found in soybeans are phytoestrogens, and they appear to reduce the incidence of breast, prostate, and colon cancers; osteoporosis; and cardiovascular disease

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation (Kurzer and Xu 1997). Carotenoids, the red, orange, and yellow pigments in tomatoes and green leafy vegetables, appear to reduce the risk of certain cancers, cardiovascular disease, and blindness caused by macular degeneration (Charleux 1996). The genetic and metabolic factors influencing levels of glucosinolates, isoflavones, and carotenoids from various plant sources are poorly understood, as is the appropriate level at which they should be consumed for maximum health benefits. Western diets typically contain limited amounts of these chemicals, and there is growing interest in finding ways to increase their content in food and to determine their appropriate health-promoting levels. Plant foods could also be used as edible vaccines (Langridge 2000, Walmsley and Arntzen 2000). Many seeds contain proteins that are allergenic in certain people. When these allergenic proteins are digested, small fragments derived from them are absorbed into patches of cells on the small intestine that are part of the immune system. Antibodies are produced against these proteins, and this leads to an immune response in the individual, with potentially severe consequences after subsequent exposure to the allergenic proteins. This same process can be used to create immunity against common viral and bacterial pathogens by producing antigenic proteins derived from them in edible plant parts. Of particular interest are a group of pathogens—Norwalk virus, Vibrio cholerae (the cause of cholera), and enterotoxigenic Escherichia coli (a source of “traveler’s diarrhea”)—that cause the deaths of several million children each year, mainly in developing countries. Preliminary studies indicate that uncooked plant foods, such as potatoes or bananas, can be used to produce pathogen-derived proteins (such as virus coat proteins). These foods might then be used to inoculate children and adults against a variety of common diseases. Although a great deal of research remains to be done to demonstrate the efficacy and economic viability of this approach, results from preliminary experiments are promising. There is also interest in using plants to produce human monoclonal antibodies. Preliminary research has demonstrated that several types of plant tissues, including seeds and leaves, have the capacity to express genes encoding the protein subunits of monoclonal antibodies and assemble them into functional complexes (Daniell et al. 2001). It remains to be seen whether plants can produce these antibodies in sufficient quantities to meet therapeutic requirements. However, if it proves possible, the technology has tremendous potential because of the expense of producing monoclonal antibodies in mammalian tissue cultures. It would be essential to grow these plants in restricted locations, but the value of the products would easily be sufficient to offset the cost of growing the crop in isolation.

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation These various modifications to foods raise a number of issues, many that are beyond the scope of this study. One class of modifications addresses nutritional deficiencies by increasing the concentration of the deficient nutrient or precursor in the plant. As an analysis of vitamin A deficiencies suggests (Nestle 2001), alleviating such deficiencies may require more than merely increasing the nutrient in a food. A careful, considered approach to using biotechnology to address nutrient deficiencies might start by considering all alternatives and developing a systemic approach to alleviating the deficiency in the identified population. A second class of modifications aims to optimize food quality by incremental improvements. Again, it may be difficult to know that an anticipated improvement in food quality will actually lead to an improvement, such as changing the content of “health-producing” compounds in plants, rather than a decline in human well-being. Clearly there are many questions that other scientists, including nutritionists and public health specialists, need to engage to ensure that biotechnology will lead to improved human health. All of these future products raise parallel questions related to environmental impact. There might be indirect human health risks mediated through the environment that would require new expert analysis. Nontarget risks associated with these plants with altered nutritional characteristics (both macronutrients and micronutrients), increased concentrations of “health-producing” compounds, or edible vaccines may be considerably more subtle than the direct mortality risks associated with plants producing insecticidal toxins, which are being evaluated presently. Mitigation of Environmental Pollution In the future, transgenic plants may be grown for reasons other than commercialization. For example, it has been proposed that transgenic plants could contribute to removing or detoxifying heavy metal pollutants in contaminated soils (“phytoremediation”). A particular problem in some locations is mercury. Plants have already been created that can accumulate mercury. Thus, growing such plants is a potential solution for cleaning up mercury pollution at despoiled sites (Pilon-Smits and Pilon 2000). This example is discussed in detail below. Finding 7.1: For predicting environmental risks of future plant varieties and their novel traits, currently commercialized transgenic crops offer only limited experience and understanding. Finding 7.2: The production of nonedible and potentially harmful compounds in crops such as cereals and legumes that have traditionally been used for food creates serious regulatory issues.

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation Finding 7.3: With few exceptions, the environmental risks that might accompany future novel plants cannot be predicted. Therefore, they should be evaluated on a case-by-case basis. Finding 7.4: In the future many crops can be expected to include multiple transgenes. Potential Environmental Impacts of Novel Traits The Animal and Plant Health Inspection Service (APHIS) appropriately refrains from speculation on environmental risks associated with crops that may or may not reach the stage of commercialization. Full and fair discussion of such risks presupposes information that cannot be known until a functional phenotype has been developed and grown in limited field trials. However, a brief discussion of the general issues associated with some new crops currently being developed will help frame the context in which environmental risks from commercialization of the next generation of transgenic crops may be discussed. Tolerance to Abiotic Stresses Abiotic stresses significantly limit crop production worldwide. Cumulatively, these factors are estimated to be responsible for an average 70% reduction in agricultural production (Bresson 1999). Drought stress not only causes a reduction in the average yield for crops but also causes yield instability through high interannual variation in yield. Globally, about 35% of arable land can be classified as arid or semiarid. Of the remainder, approximately 25% consists of drought-sensitive soils. Even in nonarid regions where soils are nutrient-rich, drought stress occurs regularly for a short period or at moderate levels. Furthermore, it has been predicted that in the coming years rainfall patterns will shift and become more variable due to increased global temperatures. Thus, improved stress tolerance may improve agricultural production. Research to create crop plants that are transformed to tolerate abiotic stresses, such as heat, drought, cold, salinity, and aluminum toxicity, is ongoing. Current research efforts in drought tolerance include the isolation of crop plant mutants to understand the molecular basis for salt responses (Borsani et al. 2001), studies on the transduction network for signaling guard cell responses and their subsequent control of carbon dioxide intake and water loss (Schroeder et al. 2001), and genetic activation and suppression screens that influence interrelationships among multiple signaling systems that control stress-adaptive responses in plants (Hasegawa et al. 2000). The actual development and field testing of novel crop plant varieties is likely to be 5 to 10 years in the future owing to the

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation environmental risks of transgenic crops has figured prominently in Europe, European pronouncements on the precautionary principle neither offer a specific evaluation of transgenic crops nor provide language that would give regulators specific instructions on how to take a precautionary approach with respect to transgenic crops. The March 12, 2001, revision to EU Directive 90/220 states that the requirements of the Biosafety Protocol, including the precautionary principle, should be respected. The 2001 directive indicates that the precautionary principle was taken into account in the drafting of the directive and must be taken into account when implementing it. Consequently, the directive does not provide a statement of the precautionary principle but identifies regulatory processes that are precautionary. It is beyond the scope of this report to provide a detailed analysis of this new directive, but suffice it to say that the precautionary principle has been incorporated into at least the labeling and traceability standards, the monitoring standards, and the EU approval process. Much the same as in the Biosafety Protocol, the precautionary principle will be defined in Europe through its application to specific cases. U.S. discussion of the precautionary principle has been sparked by both these European developments and the publication of papers from a 1998 working group conference on the meaning and applicability of the precautionary principle in a number of legal and public health settings (Raffensperger and Tickner 1998). This collection of essays on the precautionary principle includes a number of interpretations and applications, all of which should be regarded as supportive of the precautionary principle and the precautionary approach. There is considerable variation even among contributors to Raffensperger’s and Tickner’s book advocating implementation of the precautionary principle. Cranor (1998) focuses on the need to emphasize the minimization of type II statistical errors in science intended for regulatory application. Ozonoff (1998) argues that the precautionary principle should be interpreted as a screening device to apply “scientific evaluations to situations where the proportion of cases that are hazards is high and/or use methods with high specificity, that is, that correctly identify ‘no-hazard’ situations” (104). Arguably, these approaches simply reflect the current regulatory philosophy in place for transgenic plants under the coordinated framework. However, other contributors explicitly advocate the use of nonscientific criteria, such as political solidarity or respect for life, to evaluate the possibility and potential for environmental hazards (Bernstein 1998, M’Gonigle 1998). In summary, a number of different formulations are given for the precautionary principle. Advocacy of a precautionary approach can be interpreted to convey a need to reconsider and possibly strengthen regulatory oversight of technology. One key is the advocacy of statistical and

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation scientific evidentiary decision standards that err on the side of preventing serious and irreversible health and environmental effects, even in the absence of definitive demonstration of harm to humans or non-target organisms. Given the ambiguity in its various formulations as well as opportunities to interpret the seriousness of environmental hazards in different ways, the precautionary principle does not provide a single alternative to existing regulatory policies for the U.S. government. Indeed, some interpretations of the precautionary principle would be consistent with current approaches. Nor does the principle provide unambiguous guidance for the evaluation of transgenic crops. While both advocates and critics of the precautionary approach appear to have assumed that this would result in an adverse evaluation of transgenic crops (Carr and Levidow 2000, Miller and Conko 2001), it is not necessary that such a result would follow. A more definitive evaluation of the precautionary principle must await more specific criteria for its application in agriculture (Soule 2000). For the meantime, the “precautionary principle” should be regarded as a number of potential regulatory approaches pertaining to the use of science to formulate public health and environmental policy, rather than a specific proposal for change. However, as it is applied in Europe and under the Biosafety Protocol, its meaning will become clear. As it gains clarity, there may be significant implications of its use with respect to U.S. regulatory policy. Finding 7.11: The precautionary principle forms an important but imprecise context for the regulation of future transgenic organisms. Raising the Regulatory Bar It will soon become necessary to reconsider the general philosophy of regulation for environmental impact that has been applied to all forms of agricultural technology since World War II. Plant scientists have developed an array of techniques for introducing genetic novelty into crop varieties through conventional breeding methods such as mutagenesis, wide crosses, and embryo rescue. These techniques have the potential to introduce genes and genetic variations into crops that in some cases equal the novelty associated with recombinant DNA techniques. It is entirely possible that crops developed with either of these techniques could possess phenotypic traits associated with elevated levels of environmental risk. As BOX 1.1 notes, Green Revolution varieties that increased commercial crop capacity to utilize nitrogen fertilizer shifted land-use patterns and sparked a worldwide increase in the adoption of chemical inputs. A comparison of the environmental risks from Green Revolution varieties

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation with those of the first, second, or third generations of transgenic crops would be a highly speculative enterprise. Yet in retrospect it is difficult to argue that Green Revolution impacts on the environment were automatically safe, benign, or even acceptable simply because they were developed using conventional breeding. With the potential for introducing additional novel traits through nontransgenic methods, it becomes increasingly difficult to defend the idea that conventional crops should automatically be excluded from scrutiny for environmental impact. As noted earlier, NRC reports have consistently found that use of recombinant DNA technology in the development of an agricultural crop does not in itself create a new class of risks. As with conventionally bred crops, it is the phenotypic characteristics of the plant that are the source of environmental risks. This report and the 2000 NRC report (2000c) on pest-protected plants cite a number of environmental risks that should be accounted for in the regulation of both current and future crop varieties. When these observations are combined, the possibility that nontransgenic crops may also pose environmental risks requiring a regulatory response becomes logically inescapable. Yet new crop varieties posing potential hazard fail to require regulatory scrutiny under APHIS while potentially benign transgenic crops do because APHIS oversight excludes conventional crops. Those plants produced via recombinant DNA are regulated, and those produced by other methods are exempt, even if the final product has an identical phenotype and therefore presents similar potential risks. Moving beyond the realm of crop modification, it is also clear that the bar has been raised substantially for acceptable environmental effects for novel pesticides and new agricultural practices (e.g., changes in crop rotations and changes in cultivation practices). As our perspective on the ecological interactions and interchange between agricultural and nonagricultural lands evolves (see Chapter 1), the environmental standard being set for transgenic plants may be a better overall environmental effects model for agriculture than the model developed in the early 1900s for assessing the acceptability of conventional crop varieties and agricultural practices. Although government regulation of conventionally modified plants has been virtually nonexistent, the agricultural research establishment has not ignored the potential of genetic modification of crops to result in environmental change. Indeed, some of the work begun in the 1960s to assess the long-term impacts of Green Revolution cultivars and cropping practices demonstrated insight into the needs for examining environmental effects on long and large scales. As discussed in Chapter 1, it was only because of long-term 30-year experiments on the impact of cropping intensification that researchers were able to clearly document the effects of

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation the new cropping practices on soil characteristics. These long-term experiments were sponsored by nonprofit groups and local governments. Today, most efforts at examining environmental impacts of transgenic crops emphasize short-term laboratory and field plot experiments. While such experiments are useful, there is a need to examine effects that cannot be seen at such small scales. For example, short-term and small-scale experiments would not have predicted the effects of Green Revolution practices on lowering the water table in semiarid regions of India or the rise in water tables in other areas that has been accompanied by salinization of the soils in the root zones of crops. Finding 7.12: The environmental impacts of transgenic plants and other new agricultural practices can be studied at a number of ecological scales ranging from the specific toxicological effects of a newly produced compound to the large-scale and long-term spatial and temporal effects of changes in agricultural practices induced by the introduction of a novel crop variety. Finding 7.13: Currently APHIS environmental assessments focus on the simplest ecological scales, even though the history of environmental impacts associated with conventional breeding points to the importance of large-scale effects, as seen in the impacts of Green Revolution cultivars. Recommendation 7.1: APHIS should include any impact on regional farming practices or systems in its deregulation assessments. Society demands that commercial products are deemed safe for health and the environment. The public trusts government regulators to assess risks adequately, to exclude from commerce products posing unacceptable risks, and to impose appropriate risk management strategies to reduce risks. Some people want regulators to test “everything for everything” prior to commercial release. All regulatory agencies, including APHIS, must work with limited financial, temporal, and human resources, so testing everything is not feasible. Instead, prudence and fiscal reality dictate that regulators identify those products most likely to be hazardous and concentrate scrutiny on them, applying a science-based approach to risk assessment. Currently, one of the risk-based triggers for assessment of a crop by APHIS is that it is a transgenic crop variety (see Chapter 2). This trigger captures all products of genetic engineering but excludes potentially hazardous products derived from conventional methods. This regulatory trigger is imperfect because it does not provide regulatory scrutiny for certain conventional crop plants that may have environmental risks. As discussed more thoroughly in Chapter 2, it fails to capture potentially

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation hazardous conventional products, such as stress-tolerant canola. At the same time, it brings under regulatory scrutiny some transgenic crop plants that it later determines to have no significant environmental risks. Indeed, an intraspecific recombinant DNA variety would be regulated even if the gene were removed and replaced back in its original location with no extraneous DNA. Thus, there are reasons for considering other or additional potential triggers for the regulation of crop varieties. APHIS has the authority to regulate all plants that pose a plant pest risk under its present statutory authority. On May 25, 2000, the U.S. Senate and House of Representatives agreed on a conference report on a new Plant Protection Act (PPA), which was developed to improve the government’s ability to prevent and mitigate the effects of organisms that might harm agriculture and the environment. This act, signed by President Clinton, on June 20, 2000, includes products of genetic engineering but is not limited to them. The PPA offers an opportunity for APHIS to refocus regulation on those plant products that pose risk, regardless of the method of derivation. As developed in more detail in Chapter 2, however, scientifically defensible ex ante risk assessment is not yet possible, so it will not be possible to develop a science-based trigger based solely on predictions of the risks associated with particular crop varieties. In addition, it would be imprudent to bring all conventional crop varieties under regulatory oversight. Thus, careful scientific thought must be applied to this problem to avoid extraneous regulation. Finding 7.14: The committee finds that the Plant Protection Act of 2000 can be viewed as an opportunity to clearly define the types of novel plants, regardless of method of breeding, that trigger regulatory scrutiny. As explained in previous chapters, APHIS regulates transgenic plants under the authority of the Federal Plant Pest Act (FPPA) and the Federal Plant Quarantine Act (FPQA). While the scope of these acts is quite broad, there are some taxonomic and functional limits that make regulation of some potentially hazardous organisms problematic. For example, the FPPA does not recognize vertebrates as pests. Furthermore, transgenic plants that have been modified using Agrobacterium DNA or the DNA from certain viral species fall clearly within the regulatory authority of the FPPA because these organisms are plant pests. Although APHIS can regulate plants that have been genetically transformed without the use of DNA from a plant pest, determining which plants will be regulated is not simple. As identified early in this report, the regulatory options available to APHIS through the FPPA are limited. For example, once a plant is deregulated, APHIS has no authority to restrict its use or to even monitor it.

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation The broad language of the new Plant Protection Act defines “plant pest” as including all vertebrate and invertebrate animals except humans. The PPA repeals the FPPA and the FPQA, however, it provides for regulations issued under the repealed acts to be enforced until new regulations are developed. The PPA also provides the potential for developing new procedures for regulating plant products that pose risk. For example, regulations could presumably be written giving directives to APHIS on how to involve the public and external scientific experts in its review process. In addition, regulations under the PPA could be used to provide the flexibility lacking in present regulations. For example, it would be useful to allow APHIS to recall or rescind deregulated plants under appropriate circumstances. Current federal policymakers will determine to what extent the new PPA will be used as a vehicle for change. Recommendation 7.2: The committee recommends that the Plant Protection Act of 2000 be viewed as an opportunity to increase the flexibility, transparency, and rigor of the APHIS decision-making process. Finding 7.15: Nontransgenic crop breeding techniques have the potential to introduce genes and genetic variation into crops that equal or surpass the novelty associated with recombinant DNA techniques. It is entirely possible that crops developed using these techniques could possess phenotypic traits associated with elevated levels of environmental risk. When evaluating transgenic crops for deregulation, it becomes increasingly difficult to defend the idea that these new nontransgenic crops should automatically be excluded from scrutiny for environmental impact. THE NEED FOR STRATEGIC PUBLIC INVESTMENT IN RESEARCH Perhaps more than anything else, the experience with commercialization of transgenic crops has revealed gaps in the knowledge base for understanding and measuring the environmental risks of crop production, irrespective of whether recombinant DNA technologies have been applied. Crops developed through nontransgenic methods can and have resulted in avoidable environmental damage. Managing the risks of crop production in the future will depend on improving basic scientific knowledge and research capacity with respect to five key areas discussed below.

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation Improved Risk Analysis Methodologies and Protocols Formal research support in the United States for the study of environmental impacts of transgenic plants has been sparse. The longest continuous funding, now almost a decade, has come from the USDA’s Biotechnology Risk Assessment Research Grants Program (BRARGP) to assist federal regulatory agencies in making science-based decisions about the safety of introducing genetically modified organisms into the environment. The program accomplishes its purpose by funding scientific research in priority areas determined in part by the input of the regulatory agencies. Research proposals submitted to this competitive grants program must address risk assessment, not risk management, and are evaluated by a peer panel of scientists. The program has allocated no more than a few million dollars for research each year. Recently, the USDA’s Initiative for Future Agriculture and Food Systems (IFAFS) program has included a competition for funding research, education, and extension on the management of environmental risks of agricultural biotechnology. Both funding programs have substantial limitations—BRARGP because its focus is only on assessment and because the total amount of funding is so low; IFAFS because the focus is only for risk management and the funding program itself is anticipated to have a short life. Neither program funds monitoring or research related to monitoring. Research on the environmental impacts of transgenic plants can be accomplished through other funding sources if the research questions asked have general significance. For example, issues directly associated with the impacts of transgenic plants may often be associated with critical, but largely unanswered, questions in other fields. For example, whether or not the introgression of pest resistance transgenes into wild populations will result in the evolution of weediness or invasiveness is directly associated with important questions in population biology regarding the genetic and ecological causes and correlates of invasiveness (Traynor and Westwood 1999). There are several critical areas of research related to risk analysis that would benefit from increased funding. In the area of hazard identification and risk assessment, there is a need for improved, scientifically sound protocols to detect effects of transgenes and transgene products on non-target organisms. Present protocols are better adapted for screening for effects of toxic chemicals with broad ecological effects, rather than biologically released materials with more targeted specificity. This includes better understanding of effects on pollinators, natural enemies, species of conservation concern and soil organisms. There is also a need for improving understanding of the environmental effects of transgene

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation movement. Present research has concentrated on determining the conditions under which transgene movement would likely occur. It will be essential to develop a deeper theoretical and empirical understanding of the kinds of environmental effects that could result from transgene movement and the conditions under which such effects are likely to occur. This needs to be understood for transgene movement associated with pollen, viruses, and bacteria. In addition, there is a need to develop assessment protocols that can identify the circumstances under which a plant is likely to become invasive. Because deliberate introduction of plants is the most common route of establishment of invasive plants, it will be critical to understand how genetic modification affects invasiveness. Research on the effectiveness and efficiency of present regulatory systems is needed to develop approaches to enable the regulatory systems to improve based on scientific principles and data as they acquire information and experience. This includes analysis of alternative methodologies as discussed in Chapter 2. Research is needed to evaluate the environmental risks associated with conventionally produced crop plant varieties. This will involve understanding the kinds of risk and the circumstances under which these risks might occur. Because conventional crop breeding methods are constantly changing, this evaluation should include a dynamic assessment. Because many novel transgenic organisms are likely to be developed in the future, it will be useful to fund research to identify and investigate possible environmental hazards associated with these new types of transgenic organisms. These efforts might best be initiated several years before any of these plants become likely to be commercialized. This research effort could be coordinated with research on transgenic methods to minimize risk, as discussed below. Postcommercialization Validation and Monitoring As discussed in Chapter 6, there is a need for formal postcommercialization validation testing to determine if the results of small-scale precommercialization tests are relevant at larger spatial and temporal scales. The infrastructure for such testing exists but resources must be targeted to carry out such testing in a rigorous manner. Development of long-term monitoring systems, and development and coordination of trained observer monitoring will require a major commitment to building infrastructure. Long-term monitoring is based on the use of ecological indicators (NRC 2000a), which are intended to provide valid, reliable, and cost-

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation effective information about the status of important ecological systems. Repeated observations of these indicators can enable the identification of associations between changes in indicator values and the use of transgenic crops. To improve long-term monitoring of transgenic crops, research is needed to fill knowledge gaps related to ecological indicators. Important research areas include temporal behavior of ecological indicators, and the need for improvements in mechanistic understanding of the links between ecological dynamics at population and other levels and the ecosystem process measures frequently used as indicators. The latter area is particularly important to ensure that ecological indicators will be able to resolve the ecological effects of transgenics from the effects of other factors that may be associated with the use of transgenic crops. There also are important research questions about the structure and organization of scientific efforts to accomplish long-term monitoring. For example, how should feedback loops be established between validation efforts and long-term monitoring efforts so as to clarify the adequacy of available ecological indicators for monitoring of ecological effects of transgenic crops? Finally, research is needed on processes for establishing long-term monitoring indicators in relation to transgenic crops as well as research to evaluate the efficacy and effectiveness of potential long-term indicators. Trained observer monitoring attempts to detect effects the transgenic crops that are so poorly understood—or simply unforeseen—that they cannot yet be the target of more specific monitoring efforts. The goal is to develop a network of trained observers that could detect effects of this sort. The outstanding research needs related to this kind of monitoring concern questions about what sort of practical approaches could serve this purpose, as well as the broader challenge of “posting” observers that can monitor environmental effects of technological change in agriculture generally, since it is unlikely that monitoring aimed solely at transgenic effects will be cost effective. Specific research needs include improving understanding of the organization and facilitation of observer activities that are or could be performed by existing organizations that have a current or potential interest in performing relevant ecological monitoring (e.g., the Christmas Bird Count of the National Audubon Society). Another important issue is the structure and functioning that would provide integration, organization, and development for the trained observer network. Many questions remain about how such a network would perform its functions—for example, proactively conducting two-way communication about monitoring issues with interested parties in organizations that do monitoring, developing curricula for training sessions for observers, providing a clearinghouse for reports of notable observations from field monitoring efforts, and developing quality assurance standards.

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation Improved Transgenic Methods to Reduce Risks and Improve Benefits to the Environment Some of the concerns raised about early biotechnology-derived crop varieties can be avoided in the future with our expanding knowledge base. For example, pollen flow issues could be reduced if there are advances in plastid transformation, if sterility systems are engineered into the varieties, or if gametophytic factors (i.e., genes expressed in the pollen or egg) can be used to restrict fertilization of the egg. As nontissue culture methods are developed for gene transfer, such as cocultivation of developing flowers with A. tumefaciens (see Chapter 1), gene transformation in a number of plant species might become much less genotype dependent, perhaps even to the point of using an elite cultivar for the initial transformation event, thus avoiding linkage drag as the result of subsequent breeding procedures. In addition, tissue culture itself often introduces unwanted and unpredictable genetic and epigenetic variation to transgenic plants that such methods may avoid. Alternatively, different promoters could allow greater control of where in the plant the gene product is produced; tissue-specific promoters could preclude expression of pesticidal proteins, for example, in pollen and other tissues. Temporal and spatial regulation of gene expression also can be controlled sometimes via an exogenous inducer. The ability to identify and transfer genes from elite germplasm collections of the same species could dramatically improve as a result of knowledge gained from genomics and proteomics research. Antisense technology will improve our ability to knock out the function of expressed genes. Targeted recombination and gene replacement technologies can be expected to improve, which will allow greater precision in gene insertion following transformation. Our ability to produce primary transformation events with selectable markers that can be removed through genetic crosses or that make use of benign (more acceptable) selectable markers will be enhanced. Improvements in DNA sequencing already allow the full sequence analysis of primary transformation events, such that optimal ones with simple single-gene insertions are selected early in the process of engineering transgenic traits. Value-Oriented Research When new technologies are involved in large-scale social changes, public debate and opinion formation on value-based issues can be facilitated by research that articulates and analyzes ethical, legal, and cultural traditions as they might bear on novel questions, as well as more traditional economic research on costs, benefits, and likely effects on the prices

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Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation and availability of food. Such research helps both scientists and the public understand what is at stake and how the issues might be viewed from differing perspectives. The potential for economic and sociological research has been well established in agriculture, and there is clearly a need for more studies that focus on biotechnology. The potential for philosophical, legal, and culturally-oriented research on issues in involving genetics has been demonstrated by the Ethical, Legal, and Social Issues (ELSI) program associated with the Human Genome Initiative. This program has produced both scholarly studies and educational materials that help people go beyond initial reactions of enthusiasm or repugnance. The USDA has funded little research of this kind, and few U.S. colleges of agriculture offer training or coursework to prepare professionals for ethical decision making—coursework that is now routinely offered in medical schools. The possibility cannot be dismissed that at least some of the controversy and turmoil that have greeted genetic engineering in agriculture is due to this omission. The USDA should encourage the development of a systematic program of research and teaching on ethical, legal, and cultural dimensions of agriculture and food issues, especially as they involve genetic techniques. Recommendation 7.3: Significant public-sector investment is called for in the following research areas: improvement in risk analysis methodologies and protocols; improvement in transgenic methods that will reduce risks and improve benefits to the environment; research to develop and improve monitoring for effects in the environment; and research on the social, economic, and value-based issues affecting environmental impacts of transgenic crops.